Pearl millet is a climate-resilient, nutritious crop with low input requirements that could provide economic returns in marginal agro-ecologies. In this study, we report quantitative trait loci (QTLs) for iron (Fe) and zinc (Zn) content from three distinct production environments. We generated a genetic linkage map using 210 F6 recombinant inbred line (RIL) population derived from the (PPMI 683 × PPMI 627) cross using genome-wide simple sequence repeats (SSRs). The molecular linkage map (seven linkage groups) of 151 loci was 3,273.1 cM length (Kosambi). The content of grain Fe in the RIL population ranged between 36 and 114 mg/Kg, and that of Zn from 20 to 106 mg/Kg across the 3 years (2014–2016) at over the three locations (Delhi, Dharwad, and Jodhpur). QTL analysis revealed a total of 22 QTLs for grain Fe and Zn, of which 14 were for Fe and eight were for Zn on three consecutive years at all locations. The observed phenotypic variance (R2) explained by different QTLs for grain Fe and Zn content ranged from 2.85 (QGFe.E3.2014–2016_Q3) to 19.66% (QGFe.E1.2014–2016_Q3) and from 2.93 (QGZn.E3.2014–2016_Q3) to 25. 95% (QGZn.E1.2014–2016_Q1), respectively. Two constitutive expressing QTLs for both Fe and Zn co-mapped in this population, one on LG 2 and second one on LG 3. Inside the QTLs candidate genes such as Ferritin gene, Al3+ Transporter, K+ Transporters, Zn2+ transporters and Mg2+ transporters were identified using bioinformatics approaches. The identified QTLs and candidate genes could be useful in pearl millet population improvement programs, seed, restorer parents, and marker-assisted selection programs.